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A thousand bites: Insect introductions and late Holocene environments
Citation for published version: Panagiotakopulu, E & Buckland, PC 2017, 'A thousand bites: Insect introductions and late Holocene environments', Quaternary Science Reviews, vol. 156, pp. 23-35. https://doi.org/10.1016/j.quascirev.2016.11.014
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1 A thousand bites – Insect introductions and late Holocene environments
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3 Eva Panagiotakopulua*, Paul C. Bucklandb
4 a. School of Geociences, University of Edinburgh, EH8 9XP, UK
5 b. 20 Den Bank Close, S10 5PA, Sheffield, UK
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7 *Email: [email protected]
8 9 Abstract 10 11 The impact of insect species directly associated with man-made habitats and human dispersal 12 has been, and remains globally significant. Their early expansion from their original niches 13 into Europe is intrinsically related to discussions of climate change, origins of domesticated 14 plants and animals, the spread of agriculture and infectious diseases. The Holocene fossil 15 records of the dispersal of three storage pest species, Sitophilus granarius, Oryzaephilus 16 surinamensis, and Tribolium castaneum, the housefly, Musca domestica, and the human flea, 17 Pulex irritans from 221 sites have been mapped ranging from the Near East to Europe and 18 from the Neolithic to the post medieval period. The importance of human induced change as 19 a driver for the spread of synanthropic faunas and the potential for the spread of disease 20 during this process are discussed. The results show links between mobility of farming groups 21 and distribution of synanthropic insect species and produce a roadmap for the different 22 cultural periods of the Late Holocene based on dispersal of these synanthropic insects. During 23 the Neolithic, the first wave of insect introductions shows the northern European frontiers of 24 storage of cereals, introduction of domestic animals and pastoralism and exchange. Pest 25 introductions, linked with the itinerary of the Roman army, reached the most northerly parts 26 of the Empire. During the medieval period, the insect records indicate further expansion and 27 changes which parallel the spread of epidemic diseases like Plague. Understanding the 28 timing and the rates of change of synanthropic insects provides key information about the 29 development of the homogenised and highly anthropogenic environments in which we live 30 today. 31
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32 33 Keywords: Holocene, fossil insects, human impact, Europe, biogeography, pests, disease 34 35 36 1. Introduction 37 38 Domestication of animals and plants inevitably also involved a suite of insects able to exploit 39 man-made habitats which closely mimicked those occupied in the wild, in some cases to the 40 extent that their ‘natural’ habitats are largely unknown. Several of these almost casual 41 invasions involved the assisted crossing of Wallacean boundaries, but many others involved a 42 more subtle shift from beneath bark, for example, into food stores, or from animal dung in 43 relatively warm countries to warm manure heaps in colder places Ultimately, many have had 44 global impacts on biogeography and initiated a new range of relationships, from parasitic to 45 symbiotic and commensal, as part of the relatively newly created synanthropic environments 46 (cf. Simberloff et al., 2013). Whilst the primary domesticates have been the subject of 47 frequent review and discussion in the archaeological literature (most recently, see Colledge et 48 al., 2013) and the history of vertebrate pests has been extensively studied (cf. Aplin et al., 49 2012; Jones et al., 2012), other invaders have tended to be only viewed in the recent 50 timeframe, with only rare recourse to the fossil record. The spread of a range of species with 51 man over this longer timeframe is in many cases linked with episodes of landscape clearance 52 and the creation of culturesteppe, an aspect well documented in the distribution of open 53 ground beetles (cf. Andersen, 2000), and occasionally discussed with regard to the fossil 54 record (e.g. Dinnin and Sadler, 1999; Eriksson, 2013).
55 Whilst Frans Vera (2002) has sought to impose a more dynamic model on the European 56 Holocene landscape, the primary threshold in terms of inexorable and irreversible 57 biogeographic change is provided by the moving boundary of the Neolithic (Colledge et al., 58 2013), replacing hunting, fishing and gathering, often rapidly and almost exclusively, with 59 crop production and storage. Climate change has been hypothesized as one of the main 60 drivers behind this transition (e.g. Sherratt, 1997), while other factors, for example, 61 population rise and its consequences (Rowley-Conwy and Layton, 2011; Lemmen, 2014), 62 and cultural diversity may also have led to innovation and change (Kandler and Laland, 63 2009). From the viewpoint of the insect and other fellow travellers, the lack of detailed 64 datasets for the Neolithic, coupled with the limitations of dating, precludes definitive answers
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65 and inevitably any earliest occurrence is likely to be eventually overturned, although DNA 66 research offers the possibility of tracing pathways and origins (cf. Jones et al., 2012). A 67 considerable part of the debate, with DNA recently producing useful data about mobility of 68 human populations (Bramanti et al., 2009, Pinhasi et al., 2013), has focussed on the patterns 69 of spread of domestication and agriculture. The current consensus points to dispersal of both 70 plants and terrestrial mammals from a number of different foci (Larson et al., 2007, Brown et 71 al., 2008). Other organisms, including insects, have also had a part in this process. In 72 addition to intentional introductions as part of domestication, the Neolithic is the primary 73 threshold for a number of unintentional introductions, including field, storage and household 74 pests and ectoparasites on humans and their animals (e.g. Panagiotakopulu 2000, 75 Panagiotakopulu 2001; Buckland 1981, 1991; Buckland and Sadler, 1989). In turn, these 76 contributed either directly or indirectly to the spread of new pathogens, harboured in the 77 reservoirs created by sedentary lifestyle and associated activities (Martin, 2003; 78 Panagiotakopulu, 2004a). This "package" was established with the spread of farming around 79 the Mediterranean, to central and northern Europe, before being introduced worldwide 80 (Simberloff et al., 2013; Jones et al., 2011; McMichael, 2004).
81 The timeframe of these introductions is significant, as it not only provides an independent 82 way to track human movement and the spread of farming, but also gives information about 83 the transition process from hunter gathering to farming and from small settlements to 84 urbanisation. Storage pests are linked with crop losses which periodically may pose 85 significant problems (Halstead and O' Shea, 2004; Oerke, 2006). In the archaeological record 86 such losses are often underestimated or overlooked. Thus, the timeline for the arrival and 87 establishment of pests in different areas provides a terminus post quem (earliest possible date) 88 for considering crop introductions, storage and storage losses (for example, in Roman Britain 89 (Buckland, 1978; Smith and Kenward, 2012) as part of the overall discussion). Of similar 90 importance are insect species which may be linked with disease. When it comes to 91 understanding origins and dynamics of vector borne infectious diseases (Parham et al., 2015), 92 these might be some of the few available lines of information (cf. Panagiotakopulu, 2004a on 93 the origins of Plague), but are rarely studied.
94 Within this context, by mapping the dispersal of selected introduced insect species, this paper 95 aims to systematically examine the role of these species as proxies for understanding the 96 development of synanthropic environments, conditions for potential spread of disease and to 97 look into their spread in relation to human mobility and exchange.
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99 2. Methodology
100 The insect species considered have been selected on the basis of their importance, abundance 101 of fossil records and continuity over different periods of the Late Holocene. They cover a 102 range of synanthropic habitats and they have different areas of origin. Three species of 103 Coleoptera, the primary storage pest Sitophilus granarius (L.), and the secondary pests 104 Oryzaephilus surinamensis (L.) and Tribolium castaneum (Hbst.), which are some of the 105 most significant pest species worldwide, have been selected for this study In addition, a 106 cosmopolitan fly species, Musca domestica L. and one of the most widely spread 107 ectoparasites, Pulex irritans L. are discussed in order to place their late Holocene 108 introductions in the general context of synanthropic environments and to link their presence 109 to the potential spread of disease. Their distribution was mapped during different 110 archaeological periods, from the Neolithic to the post medieval period (see Supplementary 111 Data A, Tables A1 -A8), as the bulk of fossil records come from archaeological sites. The 112 data were collated from 142 different geographic locations and 221 sites (see Supplementary 113 Data B, Tables B1-B5). Only site presence was taken into account for the purposes of this 114 paper, to avoid biases with individual species frequencies from samples from a variety of 115 contexts, diverse in terms of preservation and taphonomy. The contexts include excavated 116 houses, farms, middens, wells, contexts around settled areas, tomb offerings, material from 117 shipwrecks, etc. Mode of preservation ranged from desiccation, freezing and waterlogging to 118 calcification, charring and imprints on pottery. Published information was compiled using 119 primarily BugsCEP (Buckland and Buckland, 2006) and unpublished records were also 120 incorporated. Gaps in distribution are in part a result of poor preservation, in particular on 121 semiarid sites around the Mediterranean, and also the lack of relevant research.
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123 3. The Fossil evidence
124 Information from insect faunas associated with hunter gathering sites pre-dating agriculture is 125 rather thin and largely associated with the restricted faunas of the Arctic, with carrion species 126 and ectoparasites dominating the few relevant assemblages (see Böcher and Fredskild, 1993; 127 Skidmore, 1996). Human lice, man’s most intimate companions, have been recorded from 128 northeast Brazil around 10,000 years ago (Araújo et al., 2000) whilst from the northern
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129 hemisphere the earliest record is from the Heman Cave, in the Dead Sea region of Israel, 130 9000 years ago (Mumkuoglu and Zias, 1991), although DNA evidence points to the 131 possibility of a parasitic relationship with hominins for at least the last 70-40 thousand years, 132 (Kittler et al., 2003; Boutellis et al., 2014).
133 Human fleas Pulex irritans, on the other hand, appear to have a much shorter history with 134 man. Buckland and Sadler (1989) have argued that the primary host lay in the New World, 135 with the Guinea pig, Cavia porcellus L., domesticated in the Andes perhaps by 5000 BP 136 (Brothwell, 1983; Larson and Fuller, 2014). This, so-called human flea had reached western 137 Europe by the fourth millennium BC (Remicourt et al., 2014) (see Fig.1) and the need of the 138 species for relatively permanent ‘nests’ to maintain breeding populations links it with 139 sedentary as opposed to transient groups.
140 Away from the ectoparasites, relationships tend to be less intimate. For synanthropic Diptera, 141 true flies, their proliferation in settled areas created conditions ripe for the spread of 142 infectious diseases (cf. Greenberg, 1973). Previous papers have considered the sparse fossil 143 record of Musca domestica L., the house fly, and its association with health and hygiene in 144 human environments (Panagiotakopulu, 2004b; Skidmore, 1996). It, as other synanthropic 145 flies, is associated with the mechanical transmission of a large number of diseases, which 146 range from trachoma to typhoid, cholera, yaws and tuberculosis (Greenberg, 1973). The 147 earliest records of M. domestica, a species perhaps with origins in the Nile Valley (Skidmore, 148 1996), come from Erkelenz-Kückhoven in the Rhine Valley (Fig.1), around seven thousand 149 years ago (Schmidt, 2013). During the Neolithic, M. domestica occurs together with the 150 similarly synanthropic predatory muscid, Muscina stabulans L., at Thayngen-Weier in 151 Switzerland (Troels Smith, 1984, Nielsen, 1989). The fly Thoracochaeta zosterae (Haliday), 152 at the present day usually associated with accumulations of seaweed, also occurs on this high 153 altitude inland site (Nielsen et al., 2000); in the past it was also regularly associated with 154 latrines and manure (Webb et al., 1998).
155 Records of synanthropic insect species from the Middle East, North Africa and Europe 156 reflect domestication and farming from the Neolithic onwards. The expansion of these 157 species from their areas of origin to their northern limits (see Fig. 1) and often almost 158 cosmopolitan distribution at the present day, appears to have taken place almost coeval with 159 the spread of agriculture and sedentism. The optimal breeding temperatures of many of the
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160 pests of stored products and habitations tend to restrict them to the artificial warmth of the 161 inside of storerooms and other man-made structures in temperate areas.
162 The grain weevil, Sitophilus granarius L. is the prime example of a wholly synanthropic, 163 eusynanthropic species to the extent that natural populations have yet to be located and Plarre 164 (2010) has argued that the species evolved around the same time as the adoption of 165 agriculture. Whilst a case has been made for an origin in acorns (Howe, 1965; Weidner, 166 1983), fossil specimens have been found associated with both wheat and barley, in a Pre- 167 Pottery Neolithic well at Atlit-Yam, off the Mediterranean coast of Israel by ca. 8250 cal BP 168 (ca. 6250 cal BC) (Kislev et al., 2004), and at Dispilio in northern Greece around 7700 cal BP 169 (ca. 5700 cal BC) (Panagiotakopulu, in prep.) (Fig. 1). Buckland (1991) amongst others has 170 suggested that its primary habitat is in the seeds of wild grasses stored by rodents in the 171 region of the natural distribution of the wild ancestors of cereals across the Fertile Crescent. 172 The species is incapable of flight, but likely lived in close proximity to rodent nests and 173 human homes. This would have inevitably led to its introduction into the larger, man-made 174 caches of grain. Cold hardy but needing temperatures above 15° C to maintain breeding 175 populations, its northern limit would be set either by suitable summer temperatures or by 176 grain storage on a sufficient scale to provide heating and insulation. Buckland (1978), 177 drawing on work by Dendy and Elkington (1920), noted that one of the hazards of this insect 178 living in pit-stored grain would be the build up of potentially lethal concentrations of carbon 179 dioxide from the respiring grain.. This hazard might occasionally have prevented expansion 180 to new regions. Unlike the flightless S. granarius, relying on human agency for dispersal, 181 other members of the genus may be field pests as well as storage pests, although all require 182 higher base temperatures for flight. S. zeamais Mots. is nowadays a cosmopolitan pest of 183 maize, grain and rice (Hill, 1975) and is one of the species in the genus with the ability to fly 184 (Likhayo et al., 2000). Despite its vernacular name of ‘maize weevil’, its earliest record is 185 from Japan, from impressions in Jomon pottery, dated to ca. 10500 BP, from Sanbonmatsu, 186 Kagoshima (Obata et al., 2011); later Japanese contexts, from Kakiuchi, Kagoshima, from 187 around 4000 BP, are associated with the inception of rice cultivation in the area. The first 188 record of the rice weevil, S. oryzae (L.), which attacks all types of grain and rice (Harde, 189 1984), is from Han Dynasty tomb offerings in China dated to 185 BC (Chu and Wang, 1975), 190 perhaps an indication for the origins of the species as a pest in China; more research is 191 required, particularly from earlier contexts. Although rice is recorded from early Roman forts
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192 on the Rhine Frontier (Knörzer, 1966; Bakels and Jacomet, 2003), its eponymous weevil is 193 first recorded in Europe in early fifteenth century Southampton (Grove, 1995).
194 Similar trends are observed in the distribution of the saw toothed grain beetle, Oryzaephilus 195 surinamensis (L.), although its records are fewer compared to the granary weevil, and largely 196 Roman. Its first occurrence is from charred grain from a late Neolithic site at Mandalon 197 (4450-4340 cal BC) in northern Greece (Valamoti & Buckland, 1995). As much of the 198 synanthropic fauna, its original habitat was probably under bark, a habitat from whence there 199 are some modern records (e.g. Crowson, 1958; Zacher, 1927), and it may once have been 200 more widespread in the primeval forests of central Europe (Fig. 1). As a secondary pest of 201 damaged grain, it probably moved into the synanthropic environments after the spread of S. 202 granarius and the initial establishment of storage of cereals in central and northern Europe, 203 being picked up on the way, although there is a record, referred to by Zacher (1934) from a 204 Minoan vessel from Egypt and a further early Iron Age record from Israel (Kislev and 205 Melamed, 2000). Its present status as the most frequent pest of stored grain in Britain (Bell, 206 1991) partly reflects modern harvesting and storage methods. Roman occurrences, from 207 Masada in Israel (Kislev and Simchoni, 2007) to the Antonine Wall in Scotland (Locke, 208 2016; Smith, 2004), suggest that the support mechanisms of Rome’s armies had already 209 given it a wide synanthropic European and Near Eastern distribution by the mid-second 210 century AD. The third member of the primary triumvirate of grain pests, the flat grain beetle, 211 Cryptolestes ferrugineus (Steph.) has no pre-Roman fossil records, although again it occurs 212 from Masada (Kislev and Simchoni, 2007) to the Antonine Wall (Locke, 2016; Smith, 2004). 213 It remains widespread under bark, where it may feed on fungi (Halstead, 1993).
214 The red flour beetle, Tribolium castaneum has been noted by Whitehead (1999) in association 215 with C. ferrugineus under the flaking bark of an apple tree and this may be a primary habitat, 216 although Solomon and Adamson (1955) note that it is not cold hardy. Its earliest fossil 217 records are from Bronze Age Akrotiri, on the island of Santorini in the Aegean ca. 1744 to 218 1538 cal BC (Panagiotakopulu et al., 2013) (Fig. 1) and from Pharaonic Amarna ca. 1355 to 219 1325 cal BC (Panagiotakopulu et al., 2010). Other records begin in the Roman period, 220 extending from Mons Claudianus in the Eastern Desert of Egypt (Panagiotakopulu and van 221 der Veen, 1997) to Carlisle (Smith and Tetlow, 2009). In storage situations it is essentially a 222 secondary pest associated with processed commodities (Horion, 1965) and in northwest 223 Europe its establishment would be associated with centralised activities and larger scale food 224 processing.
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226 4. Discussion
227 4.1. Synanthropic insects and the Neolithic
228 Storage was one of the key pathways for the transition between gathering and farming and its 229 origins lie particularly in regions of seasonal climate extremes, either by drought or cold, pre- 230 dating cultivation and domestication (cf. Kujit and Finlayson, 2009). This requirement to 231 concentrate resources over lean times inevitably created abundant food reserves for species 232 previously restricted to the small stores and nests of rodents, under bark, or to the transient 233 habitats of carrion and dung. The security offered by storage was an incentive which perhaps 234 led to permanent settlements, and also provided habitats for a range of insects associated with 235 foodstuffs, faeces and other ejecta, intimately linked with man and domestic animals. 236 Humans, in addition to providing new opportunities for potential pests, also provided more 237 effective dispersal mechanisms for insects which had relied previously primarily on being 238 transported by other organisms, such as hitchhiking on fur, feathers or limbs (e.g. Woodroffe, 239 1967).
240 One result of the "Neolithic Revolution" is the spread of a strongly synanthropic insect 241 package out from early farming areas to new frontiers. This early expansion is witnessed by 242 the record of Sitophilus sp. during the 7th millennium BC, from Haçilar in Turkey from 243 Anatolia (Helbaek, 1970), onwards to the Aegean a few hundred years later. This is followed 244 by introductions in the Rhine valley, by ca. 5057 cal BC, perhaps following routes across the 245 Aegean and by the rivers of the Danube and Rhine systems. The expansion of the Neolithic 246 Linearbandkeramik (LBK) culture and associated cultivation of barley may have provided a 247 framework for introduction of the grain weevil. Whilst the emphasis on barley has not been 248 substantiated by plant macrofossil work (cf. Bickle and Whittle, 2013), to a certain extent the 249 LBK finds of S. granarius by Büchner and Wolf (1997) and Schmidt (1998, 2010) appear to 250 support this. Plant macrofossil evidence has been used to support a model of small garden 251 subsistence (e.g. Bogaard, 2005), although the planned settlements with substantial long 252 houses might equally have included centralised redistributive storage of crops. The presence 253 of S. granarius from several sites from early Neolithic Europe (Figs. 1, 2) would imply the 254 movement of cereals on a sufficient scale to maintain breeding populations. Its subsequent 255 absence north of the Alps until the expansion of Rome could be partly an artefact of available 256 samples and their taphonomy, but the early Neolithic occurrences must indicate the
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257 significance of storage for the establishment and enforcement of the LBK colonisers across 258 northern and central Europe (Figs. 1, 2).
259 In terms of pathways of introductions, in addition to the movement from the Fertile Crescent 260 to Europe, there is an indication for movement in the opposite direction, with a late Aegean 261 Neolithic record of O. surinamensis, following infestations of S. granarius, and spreading 262 from Europe southwards (see Figs. 1, 3). If anything, the records of storage pests show early 263 active networks, exchange and movement from one part of Europe to the other. In addition to 264 the establishment of S. granarius in the Rhine Valley, the wave of Neolithic introductions 265 include M. domestica, the house fly. The species is also present at Schipluiden in the 266 Netherlands (Hakbijl, 2006) and at Thayngen Weier around six thousand years ago, from 267 Neolithic Federsee (ca. 3000 cal BC) in Baden-Württemburg (Schmidt, 2004) and further on 268 from Alvastra on Lake Vättern in southern Sweden ca. 3000 cal BC (Skidmore in Lemdahl, 269 1995) (Figs. 1, 4). This provides an additional aspect of the early expansion of agriculture 270 into northern Europe; its association with manure indicates its spread together with pastoral 271 groups and their domestic animals, pushing northwards to southern Scandinavia. These early 272 introductions include the human flea with earliest records from Saint Maximin in south-east 273 France around 3600 cal BC (Remicourt et al., 2014) and Schipluiden in the Netherlands 274 around 3500 cal BC (Hakbijl, 2006). A large number of fossils of the species have been 275 recovered from Chalain ca. 3200 BC (Yvinec et al., 2000). The furthest north Neolithic flea 276 record is from Skara Brae on Orkney ca. 3100-2500 cal BC (Figs. 1, 4). Its spread has been 277 linked with the gift exchange of furs (Buckland and Sadler, 1989). These fleas were an 278 additional unwanted gift and part of the Neolithic invasion package.
279 The timing and nature of the arrival of these species in Europe, and their spread bear some 280 resemblance to the Neolithic expansion itself; in some cases it was unforced and fortuitous 281 but often it had to overcome cultural and ecological barriers (e.g. Golitko and Keeley 2007), 282 and was only forced through after several attempts.
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284 4.2 Synanthropic environments and potential for the spread of disease
285 Prior to the introduction of farming, tropical diseases, including mosquito borne diseases, as 286 well as infections associated with predation, handling of wild animals and consumption of 287 raw meat, were the primary health hazards for hunter gatherers. Neolithic farming and
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288 communal living, often shared with domestic animals, and lack of any concept of hygiene as 289 perceived in modern times, created ideal conditions for the spread of many diseases (Wolfe et 290 al., 2007). Several of these diseases are insect borne or insect associated (see Fig. 5). 291 Sedentary farming groups were periodically troubled with failure of crops and losses in 292 storage. Bad years would lead to lack of resources, or, in extreme situations, to famine, poor 293 health and death. The establishment of urban centres led to increase in demographic growth, 294 the proximity of living clusters (with all subsequent consequences, e.g. waste and sewage, 295 lack of sanitary conditions, etc.) and increase in potential disease hosts, created novel 296 opportunities for the spread of infectious disease. The mobility of farmers and their 297 menagerie brought pathogens with their hosts to new regions (cf. Semenza and Menne, 2009; 298 McMichael, 2004; Baum and Bar Kal, 2003; Wilcox and Gubler, 2005) adding infectious 299 diseases to the Neolithic package. Later, the broad range of introductions which accompanied 300 the Roman armies, as well as trade, were key changes, in terms of crossing natural 301 biogeographic barriers. Norse colonisation of the North Atlantic islands in the medieval 302 period extended this process further.
303 Although rarely studied, flies provide vital information on hygiene within settlements. The 304 introduction to Europe of house flies, known to mechanically spread a number of pathogens 305 from protozoa to viruses, during the Neolithic (Fig. 5), is important as an earliest date for the 306 spread of associated diseases to humans and a flag for potential pathogen reservoirs. Other 307 flies were also part of this process; the biting stable fly Stomoxys calcitrans L. is a carrier of 308 ricketsias Ricketsia spp., among other bacteria and parasites. This fly may also be an 309 intermediary host for helminths (Gage et al., 2008). Its remains have been found at the 310 Neolithic site of Thayngen Weier in Switzerland (Guyan, 1981).
311 As discussed above, human fleas, another disease vector for ricketsias, and a secondary 312 vector for bubonic plague (Yersinia pestis), are found relatively frequently in man-made 313 environments. Given the probability of a South American origin of the species (e.g. Dittmar, 314 2000), the Neolithic European records of Pulex irritans L. are interesting points in the 315 timeline of introductions, illustrating the rapidity with which gift exchange/trade facilitated 316 movement of potential disease vectors. After these occurrences, there are several records 317 from Amarna (1353 - 1325 BC) dating to the New Kingdom period in Egypt (Fig. 4, Table 318 B5), Iron Age in the Netherlands (Hakbijl, 1989) and the British Isles, as well as Roman 319 faunas from the British Isles (Kenward et al., 2000; see Fig. 4). There is significant difference 320 in terms of numbers of sites with flea specimens during the medieval period (Table B5),
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321 although this may be partly related to taphonomic and sampling problems (e.g. more house 322 floors being sampled, etc). It is clear that everyone, from kings and archbishops to peasants, 323 had lice and fleas at some time in the lives if not throughout. Effective flea and lice control 324 only came with the invention of the vacuum cleaner and systemic insecticides (cf. Busvine, 325 1976; Sveinbjarnardóttir and Buckland, 1983), so it could be that the fossil record reflects 326 rising urban populations driving the spread of the species. The fossil evidence indicates that 327 fleas were abundant in towns and this, in well documented disease cases as for example that 328 of Eyam in Derbyshire (Massad et al., 2004), could be the reason behind the transmission of 329 Plague to rural populations after initial urban epidemics. Even taking into account the 330 information about areas where, according to Benedictow (2010), Plague did not spread (i.e. 331 Iceland, Greenland, etc.), the numbers of medieval sites with human fleas is higher than from 332 any previous period. In northern Europe at least, the increased number of people in urban 333 centres was probably one of the reasons for the frequency of fleas (e.g. 254 individuals of P. 334 irritans from the Magistrate Court site in Hull (Hall et al., 2000)) and one of the main reasons 335 for the dimensions of the pandemic.
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337 4.3 Pest distribution and climate change
338 Most species associated with stored products are able to utilise the artificial warmth and 339 insulation provided by bulk storage, and their exposure to external temperatures is therefore 340 limited. Species associated with accumulations of waste, from manure to cess, are similarly 341 isolated, although dispersal may involve a temperature threshold, which may ultimately 342 define their range boundaries. The failure of the housefly to establish itself in Greenland 343 provides a good example. The question remains as to whether and to what extent climate 344 change was one of the drivers behind insect pest introductions or whether these were 345 primarily a result of expanding agricultural horizons. The nature of the data, which are 346 largely associated with human settlement, makes it difficult to provide a definitive answer.
347 Climate change, specifically, the end of the humid period in Africa (de Menocal, 2015) has 348 been invoked as the main reason behind the concentration of settlement and urbanisation in 349 the Nile Valley from 6000-4000 BC (Kuper and Kröpelin, 2006), however, a similar model 350 cannot be applied to the European Neolithic and cannot explain other biological invasions. 351 When it comes to insects, macroclimate is of more immediate importance for field pests, as it 352 directly affects their frequency and expansion, and related crop yields (see Bebber et al.,
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353 2013, 2014). Bad years with consequent high losses would also be indicative of climatic 354 variability affecting agricultural productivity (Tubiello et al., 2007; Rosenzweig et al., 2001), 355 although archaeological sampling is rarely sufficiently precise (cf. Panagiotakopulu et al., 356 2014). Indirectly, the distribution of storage pests may be affected by climate change. 357 Delayed onset of winter may provide a larger window for pest activity and the converse 358 would also be true. Higher temperatures during harvest, for example, may lead to "warmer 359 grain" and higher rates of infestation, and changes in precipitation and humidity as well as 360 weather extremes may also play a role (Cook et al., 2004).
361 An overview of the fossil record (Fig. 6) indicates waves of dispersal with the first 362 introductions starting in the Neolithic, during which fossil faunas included eight sites with S. 363 granarius, seven of these in Europe, and the first record of O. surinamensis (Figs. 1, 2, 3). 364 Climate could have played a secondary role for these initial introductions. The furthest north 365 of the three Neolithic records of M. domestica from Sweden, was perhaps close to the limit 366 where climate posed a barrier to the initial diffusion of agriculture in western Europe.
367 Trade in cereals and processed commodities probably sustained insect populations but the 368 evidence for insect pest introductions implies that there was limited activity in central and 369 northern Europe. During the Bronze Age there are five sites, out of ten overall, with S. 370 granarius in Europe, all of them in the Mediterranean. In the Iron Age, only two of the six 371 records were European, also in the Mediterranean (see Figs. 2, 6). In terms of introductions, 372 the Iron Age faunas included the house fly and human fleas in the Netherlands and the British 373 Isles. Although limitations (e.g. lack of research, lack of preservation) need to be taken into 374 account, the implication of the Bronze and Iron Age records is either of increased pastoralism 375 or storage which was inimical to pest survival or preservation. A sharp change took place 376 with the start of the Roman period which was characterised by a high number of sites with 377 pests. This period saw fifty five sites with S. granarius and forty one with O. surinamensis - 378 most of which are British (see Fig. 6, Tables B1, B2), a reflection on the state of research. 379 These records are probably associated with transport of food for the Roman army. The peak 380 in site numbers with relevant records could also be linked to warmer temperatures which 381 could have aided the proliferation of pests and led to significant infestations. There was a 382 similar trend during the medieval period (sixty one sites with S. granarius records and forty 383 three sites with O. surinamensis, see Fig. 6). These were accompanied by an expansion of 384 sites with human fleas, P. irritans; from eleven sites in the Roman period, all from the British 385 Isles, the record in the medieval period expands to thirty two sites. In part, as already noted,
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386 variation in site records during different periods reflects availability of samples and 387 preservation. However, if flea infestations were linked with wetter (Xu et al., 2014) or 388 warmer conditions for hosts (cf. Benedictow, 2010) or a combination of both (Stenseth et al., 389 2006), the Medieval Climatic Optimum (Mann et al. 2009; McMichael, 2011) perhaps 390 provided context suitable environments for the increase of sites with human fleas (Fig. 6). 391 The trend during the post-medieval period was for lower numbers of sites with storage pests 392 (twenty four sites with S. granarius and fourteen with O. surinamensis), while the sites with 393 fleas decline (from thirty two to eight). These changes may reflect the cooling associated with 394 the Little Ice Age.
395
396 4.4 Biological imperialism, armies and maritime trade
397 As many other pests and weeds and some crop plants (cf. van der Veen et al., 2008), the 398 expansion of the Roman Empire provided new pathways, particularly for stored product 399 pests. The pattern of introductions can be clearly seen in the British Isles, where first and 400 second century introductions of S. granarius from well - dated sites follow the footsteps of 401 the Roman army from Invasion northwards to the Antonine Wall in lowland Scotland by the 402 mid-second century AD (Dickson et al., 1979; Locke, 2016; Smith, 2004) (Fig. 7). A review 403 of the British data by Smith and Kenward (2011) reinforces Buckland’s conclusions 404 concerning the importance of scale in that S. granarius appears to be largely absent from the 405 rural landscape, while it occurred in forts and towns (see Table B1) and occasionally in larger 406 farms. One of these sites was an essentially suburban villa, at Bays Meadow, Droitwich, 407 Worcestershire (Osborne, 1977), and a second occurs in the villa at Grateley in Hampshire 408 (Campbell in Kenward, 2009), but rarely on lesser sites (but cf. Hughes, 1995). O. 409 surinamensis is found in the majority of sites with S. granarius. This period also shows a 410 number of sites containing T. castaneum, perhaps indicative of processed cereals, i.e. flour, 411 for consumption. The "red flour beetle" numbers diminish after the Roman period. King and 412 others (2014) have argued that the grain fauna in Britain all but disappeared in the post- 413 Roman period, when large scale commodity shipment largely ceased, and that this fauna 414 returned after the Norman Conquest. We would argue that this was probably not the case and 415 it overlooks the grain fauna, including S. granarius, from the late seventh century watermill 416 at Northfleet in Kent (Smith, 2011). In the absence of large scale movement and storage of 417 foodstuffs, it is probable that permanent insect pest populations were restricted to a few
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418 places where grain was milled regularly on a scale beyond that required for local domestic 419 consumption, but the problem of presence or absence of a species in a given fossil 420 assemblage is just as likely to be caused by the paucity of suitable samples. Unfortunately, 421 there is little comparative research from continental Europe, where the scale of post-Roman 422 collapse was less severe.
423 A similar pattern is evident in the early medieval period with Norse expansion, both west to 424 the North Atlantic islands and east into Russia. With the exception of Greenland, there are 425 several introductions of S. granarius and O. surinamensis to the Faroe Islands, Iceland, 426 northern Norway and the Novgorod region. Human fleas are taken to Greenland, thereby 427 completing its circumpolar distribution. Despite the presence of suitably warmed habitats in 428 middens and turf-built houses, the house fly did not reach the North Atlantic islands, where 429 its place is largely taken by the heleomyzid Heleomyza borealis Bohe. (Skidmore, 1996). In 430 both Greenland and Iceland, the preservation of insect assemblages and the number of sites 431 studied makes it possible to link the Norse settlements with assemblages specific to a hay 432 based pastoral economy. These include various other insects found outside their natural 433 distribution range which became established, sometimes ephemerally (cf. Buckland et al., 434 2009), on the North Atlantic islands in strictly synanthropic environments as part of the 435 Norse colonisation (Panagiotakopulu, 2014).
436 The development of ships which were unloaded at quaysides rather than on the beach during 437 the medieval period led to increasing numbers of on-board faunas which were only 438 occasionally offloaded when boats were cleared of dunnage and ballast (cf. Buckland, 1991) 439 The larger ships of the Hanseatic League, and the creation of their common market during the 440 late medieval period, facilitated further introductions. Although there is limited research, 441 changes in the maritime trade in the post medieval period made it possible for a range of 442 species to travel from one part of the world to the other. The first record of the house fly from 443 a ship comes from Henry VIII’s flagship the Mary Rose, sunk off Plymouth in 1545 444 (Robinson, 2005). The presence of the oriental cockroach, Blatta orientalis L. in the 445 shipwreck of the Spanish galleon San Esteban which sunk in Padre islands, Texas, in 1554 446 (Durden, 1978) give good examples of how far species can travel accidentally. The limited 447 evidence from the 18th century Dutch East Indiaman shipwreck, the Amsterdam, wrecked 448 near Folkstone in 1749, give an indication of the range of these incognito travellers. From 449 the shipwreck comes Cathartus quadricollis (Guérin-Méneville), the South American square 450 neck beetle, and the rice weevil, S. oryzae (Hakbijl, 1986), whilst the bean weevil
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451 Acanthoscelides obtectus (Say), also of New World origin, appears on Svalbard, at the Dutch 452 whaling station of Smeerenberg in the seventeenth century (Wijngaarden-Bakker and Pals, 453 1981). The huts of Barents’ overwintering station of 1596-7 on Novaya Zemlya in the 454 Russian Arctic included the blister beetle, Lytta versicatoria, although this was ground up in 455 a medicine rather than in cargo, dunnage or ballast (Hakbijl and de Groot, 1997).
456
457 5. Conclusions
458 Assessing the spread of introduced insect pest species over the longer timeframe provides a 459 different view on global ecological change as a result of human impact which recent research 460 tends to ignore (e.g. Thomas, 2013, but see Simberloff et al., 2013). The consideration of 461 past biogeography of beetle storage pests, the house fly and the human flea, provides refined 462 information which informs the discussion on the origins of the relevant species and their 463 movement into man-made environments, and reconstructs their early spread, an itinerary 464 which follows the footsteps of humans. In summary:
465 The distribution of the flightless weevil Sitophilus granarius during the Neolithic 466 provides evidence for the spread of early farming and indicates the northern limits for 467 the introduction of bulk storage of cereals.
468 The Neolithic dispersal of Musca domestica across Europe as far as southern Sweden 469 is probably associated with the mobility of agropastoral groups.
470 According to the fossil records of Oryzaephilus surinamensis, in addition to 471 introductions in northern Europe, the species was also spread southwards.
472 The long term records of synanthropic insects in northern Europe show waves of 473 introductions since the Neolithic, with peaks during the Roman and the medieval 474 period.
475 The introduction of storage pests in the British Isles during the Roman period follows 476 the itinerary of the Roman army and must be primarily associated with centralised 477 storage, redistribution and processing of cereals.
478 During the medieval period, the high number of sites with human fleas could provide 479 an explanation for the dispersal of the Black Death in Europe.
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480
481 More fossil insect research is needed in order to understand further Holocene insect 482 introductions accompanying humans, in particular from areas in Europe where the records are 483 incomplete. Filling the gaps, applying new analytical techniques on fossil assemblages, such 484 as DNA, with an emphasis on species of economic importance and disease vectors, and 485 linking the data with discussions on human mobility and insect borne diseases can provide an 486 innovative outlook on past environments.
487
488 Acknowledgments
489 Funding by AHRC and Newton Mosharafa with the grant no. AHRC/STDF AH/N009371/1 490 to EP to continue fossil insect research in Egypt including early spread of synanthropic 491 species is acknowledged. Thanks are due to the Leverhulme Trust for research awards to 492 Professor Kevin Edwards, PCB and EP, some of the results from which form part of this 493 paper. The Carnegie Trust is also acknowledged for funding. Anastasios Panayiotakopoulos 494 is thanked for his help in particular with the maps and diagrams. Last but not least we would 495 like to thank the editor, José Carrión and an anonymous referee for constructive comments to 496 the original submission which improved the paper.
497
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741 Rowley-Conwy, P., Layton, R., 2011. Foraging and farming as niche construction: stable 742 and unstable adaptations. Phil. Trans. R. Soc. B 366, 849-862. 743 Rosenzweig, C., Iglesias, A., Yang, X.B., Epstein, P.R., Chivian, E., 2001. Climate Change 744 and Extreme Weather Events; Implications for Food Production, Plant Diseases, and 745 Pests. Global Change and Human Health 2, 2, 90-104. 746 Schmidt, E., 1998. Der Kornkäfer Sitophilus granarius Schön. (Curculionidae) aus der 747 Schuttschicht des bankeramischen Brunnens von Erelenz-Kückhoven. Öst Rhein. Amtfür 748 Bodendenkmalpflege (Hg.) (Brunnen der Jungteinzeit. Internat. Symposium Erkelenz 27- 749 20 Okt. 1997). Materialenzur Bodendenkmalpflege 11, 261-269. 750 Schmidt, E., 2004. Untersuchungen von Wirbellosenrestenausjungund end neolithischen 751 Moorsiedlungen des Federsees, in: Schlichtherle, H. (Ed.),, Ökonomischer und 752 Ökologischer Wandel am Vorgeschichtlichen Federsee. Hemmenhofener Skripte 5, 753 Janus, Freiburg, pp. 160–86 . Landesdenkmalamt Baden-Württemberg, Archäologische 754 Denkmalpflege, Referat 27. 755 Schmidt, E., 2010. Insektreste aus bandkeramischen Brunnen. Tote Käfer lassen eine 756 bandkeramische Brunnenumgebung entstehen. Conference Abstract Mitteleuropa im 5. 757 Jahrtausend vor Christus, 32. Westfälische Wilhems-Universität, Münster. 758 Schmidt, E., 2013. Vorratsschädlinge im Mitteleuropa des 5. Jahrtausends, in: Gleser, H.G, 759 Becker, V. (Eds.), Beiträge zur Internationalen Konferenz in Münster 2010. Mitteleuropa 760 im 5. Jahrtausend vor Christus Bd. I8, 319-329. Münster, Berlin. 761 Semenza, J.C., Menne, B., 2009. Climate change and infectious diseases in Europe. The 762 Lancet 6, 365-75. 763 Sherratt, A., 1997. Climatic cycles and behavioural revolutions: the emergence of modern 764 humans and the beginning of farming. Antiquity 71, 271-287. 765 Simberloff, D. Martin, J.L., Genovesi, P., Maris, V., Wardle, D.A., Aronson, J., Courchamp, 766 F., Galil, B., García-Berthou, E., Pascal, M., Pyšek, P., Sousa, R., Tabacchi, E., Vila, M., 767 2013. Impacts of biological invasions: what's what and the way forward. Trends Ecol. 768 Evol. 28, 1, 58–66. 769 Skidmore P., 1996. A dipterological perspective on the Holocene history of the North 770 Atlantic Area. Unpubl. Ph.D. 771 Smith, D.N., 2004. The insect remains from the well, in: Bishop, M.C. (Ed.), Inveresk Gate: 772 excavations in the Roman civil settlement at Inveresk, East Lothian, 1996-2000 STAR 773 Monograph 7, pp. 81-88. Midlothian, Loanhead. 774 Smith, D. N. 2011. Insects from Northfleet, in: C. Barnett, J. J. McKinley, E. Stafford, J. M.
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775 Grimm & C. J. Stevens (eds.) Settling the Ebbsfleet valley: High Speed I excavations at 776 Springhead and Northfleet, Kent. The Late Iron Age, Roman and medieval landscape 3. 777 Late Iron Age to Roman human remains and environmental reports, 88-90 + Table 75. 778 Oxford-Wessex Archaeology, Oxford and Salisbury.Smith, D., Kenward, H., 2011. 779 Roman grain pests in Britain: implications for grain supply and agricultural production. 780 Britannia, 42, 243-262. 781 Smith, D., Kenward, H., 2012. Well, Sextus, what can we do with this? The disposal and use 782 of insect-infested grain in Roman Britain. Environ. Archaeol. 17, 141-150. 783 Smith, D.N., Tetlow, E., 2009. Insect remains, in: Howard-Davis, C. (Ed.), The Carlisle 784 Millennium Project: Excavations in Carlisle 1998-2001. 2. The finds, 921-925 +1481- 785 1489 on CD Lancaster Imprints 15. Oxford Archaeology North, Lancaster. 786 Solomon, M.E., Adamson, B.E., 1955. The powers of survival of storage and domestic pests 787 under winter conditions in Britain. Bull. of Entomol. Res. 46, 311-355. 788 Stenseth N.C., Samia N.I., Viljugrein H., Kausrud K.L., Begon M., Davis S., Leirs,
789 H., Dubyanskiy,V.M., Esper, J., Ageyev, V.S., Klassovskiy, N.L., Pole, S.B., Chan. K.S., 790 2006. Plague Dynamics are driven by climate variation. PNAS 103, 35, 13110–13115. 791 Sveinbjarnardóttir, G., Buckland, P. C., 1983. An uninvited guest. Antiquity 48, 32-33. 792 Thomas, C.D., 2013. The Anthropocene could raise biological diversity. Nature 502, 7. 793 Troels-Smith, J., 1984. Stall-feeding and field-manuring in Switzerland about 6000 years 794 ago. Tools and Tillage 5, 13-25. 795 Tubiello, F.N., Soussana, J.-F., Howden, S.M., 2007. Crop and pasture response to climate 796 change. PNAS 104, 50, 19686-19690. 797 Valamoti, S.M., Buckland, P.C., 1995. An early find of Oryzaephilus surinamensisL. 798 (Coleoptera: Silvanidae) from Final Neolithic Mandalo, Macedonia, Greece. J. Stored 799 Prod. Res. 31, 307-309. 800 van der Veen, M., Livarda, A., Hill, A., 2008. New plant foods in Roman Britain - dispersal 801 and social function. Environ. Archaeol. 13, 11-36. 802 Vera, F.W.M., 2002. A park-like landscape rather than a closed forest. Vakblad Natuurbeheer 803 (special issue) Grazing and grazing animals (2000): 13-15. 804 Webb, S.C., Hedges, R.E.M., Robinson, M., 1998. The seaweed fly Thoracochaeta zosterae 805 (Hal.) (Diptera: Sphaeroceridae) in inland archaeological contexts: δ13C and δ 15N solves 806 the puzzle. J. Archaeol. Sci. 25, 1253-1257. 807 Weidner, H., 1983. Herkunft einiger in Mitteleuropa vorkommender Vorratsschädlinge: 1. 808 Die Sitophilus Arten (Coleoptera: Curculionidae). [Origin of European stored product
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809 pests: 1. the Sitophilus species (Coleoptera: Curculionidae).] Mitt. Int. Entomol. Ver. V. 810 Frankfurt a. M. 8, 1–24. 811 Whitehead, P.F., 1999. Further observations on Tribolium castaneum (Herbst) (Col., 812 Tenebrionidae), especially in arboreal contexts. Entomol. Mon. Mag. 135, 76. 813 Wilcox, B.A., Gubler, D.J., 2005. Disease ecology and the global emergence of zoonotic 814 pathogens. Environ. Health Prev. Med. 10, 5, 263-272. 815 Wijngaarden-Bakker, L.H. van, Pals, J.P., 1981. Life and Work in Smeerenburg: the bio- 816 archaeological aspects. Proceedings of the International Symposium, Early Exploitation 817 of the North Atlantic, 800-1700, pp. 133-151. University of Groningen. 818 Wolfe, N.D., Dunavan, C.P., Diamond, J., 2007. Origins of major human infectious diseases, 819 Nature 447, 279-283. 820 Woodroffe, G.E., 1967. Phoretic behaviour of adult Aglenus brunneus (Gyllenhal) (Col. 821 Colydiidae). Entomol. Mon. Mag. 103, 44. 822 Xu, L., Stige, L.C., Kausrud, K., Ben A., Tamara M., Wang, S., Fang, X., Schmid, B. 823 Valentijn, L.Q. Stenseth, N.C., Zhang, Z., 2014. Wet climate and transportation routes 824 accelerate spread of human plague. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 281 (1780). 825 Yvinec J.-H., Ponel, P., Beaucournu, J.-C., 2000. Premiers apports archéoentomologiques de 826 l’étude des Puces: aspects historiques et anthropologiques (Siphonaptera). Bull. Soc. 827 Entomol. France 105, 4, 419-425.
828 Zacher, F., 1934. Vorratsschädlinge und Speicherwirtschaft im alten und neuen Ägypten. 829 Forsch. Fortschr. 10, 347-348. 830 Zacher, F., 1927. Die Vorrats-, Speicher- und Materialschadlinge und ihre Bekämpfung. 831 Berlin. 832 833 List of Figures
834
835 Figure 1. Map of origins, earliest records in years BP, and suggested early distribution of 836 Sitophilus granarius L., Musca domestica L., Oryzaephilus surinamensis (L.), Tribolium 837 castaneum (Hbst.), and Pulex irritans L. For further details, see Supplementary Tables A1, 838 A2 and Tables B1-B5.
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839 Figure 2. Fossil records of Sitophilus granarius (L.) from Palaearctic sites from the Neolithic 840 to the post medieval period. For further information on particular records and sites see Table 841 B1.
842 Figure 3. Fossil records and distribution of Oryzaephilus surinamensis (L.) and Tribolium 843 castaneum (Hbst.) from Palaearctic sites from the Neolithic to the post medieval period. For 844 further information on particular records and sites see Supplementary Tables B2, B3.
845 Figure 4. Fossil records of Musca domestica L. and Pulex irritans L. from palaearctic sites 846 from the Neolithic to the post medieval period. For further information on particular records 847 and sites see Supplementary Tables B4, B5.
848 Figure 5. Infectious diseases, including insect borne diseases, and pathways of transmission 849 from the early Holocene to the modern day, developed from an initial idea by Baum and Bar 850 Kal (2003). Synanthropic insects and ectoparasites are an important part for both creating 851 environments for the establishment and spread of disease. The chronology used is broad and 852 for the purposes of the diagram. For information on particular chronological periods and 853 records, please see Supplementary Data. 854 Fig. 6. Total numbers of sites with fossil records of Tribolium castaneum (Hbst.), Sitophilus 855 granarius (L.), Musca domestica L., Oryzaephilus surinamensis (L.) and Pulex irritans L. 856 discussed in this paper, in the context of the Late Holocene climate (from McMichael 2011). 857 For information on specific records and chronology from particular periods, see 858 Supplementary Data.
859 Fig. 7. Closely dated Roman sites with Sitophilus granarius L. in Britain indicating the 860 spread of the species with the movement of the Roman army north to the Antonine wall. 861 The records from London, Colchester, Pomeroy Wood, Dragonby and York date to the 1st 862 century AD, whilst the records from Exeter, Nantwich, Papcastle, South Shields, Bearsden 863 and Inveresk fall within the 2nd century AD. For more information please see Table B1.
864
865 Supplementary Data
866 A. Chronology 867 868 Table A1.Neolithic chronology of geographic regions mentioned in the paper.
27
869 Table A2. Bronze Age chronology of geographic regions mentioned in the paper.
870 Table A3. Iron Age timeframe of geographic regions mentioned in the paper.
871 Table A3. Roman Age of geographic regions mentioned in the paper.
872 Table A4. Post Roman Age of geographic regions mentioned in the paper.
873 Table A5. Medieval period timeline of geographic regions mentioned in the paper.
874 Table A6. Post medieval period of geographic regions mentioned in the paper.
875 876 B. Fossil records 877 878 Table B1. Palaearctic archaeological sites with fossil records of Sitophilus granarius (L.). A 879 full list of the relevant references is provided in The bibliography of Quaternary Entomology 880 collated by Buckland, Coope and Sadler (Qbib,
881 Table B2. Palaearctic archaeological sites with fossil records of Oryzaephilus surinamensis 882 (L.). A full list of the relevant references is provided in The bibliography of Quaternary 883 Entomology collated by Buckland, Coope and Sadler (Qbib,
884 Table B3. Palaearctic archaeological sites with fossil records of Tribolium castaneum (Hbst.). 885 A full list of the relevant references is provided in The bibliography of Quaternary 886 Entomology collated by Buckland, Coope and Sadler (Qbib,
887 Table B4. Palaearctic archaeological sites with fossil records of Musca domestica L. A full 888 list of the relevant references is provided in The bibliography of Quaternary Entomology 889 collated by Buckland, Coope and Sadler (Qbib,
890 Table B5. Palaearctic archaeological sites with fossil records of Pulex irritans L. A full list of 891 the relevant references is provided in The bibliography of Quaternary Entomology collated 892 by Buckland, Coope and Sadler (Qbib,
893
894 895
28
Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7